Abstract
It is counterintuitive that invertebrate shells can induce bone formation, yet nacre, or mother of pearl, from marine shells is both osteoinductive and osteointegrative. Nacre is composed of aragonite (calcium carbonate) and induces production of vertebrate bone (calcium phosphate). Exploited by the Mayans for dental implants, this remarkable phenomenon has been confirmed in vitro and in vivo, yet the characteristic of nacre that induces bone formation remains unknown. By isolating nacre topography from its inherent chemistry in the production of polycaprolactone (PCL) nacre replica, we show that, for mesenchymal stem cells, nacre topography is osteoinductive. Gene expression of specific bone marker proteins, osteopontin, osteocalcin, osteonectin, and osterix, is increased 10-, 2-, 1.7-, and 1.8-fold, respectively, when compared to planar PCL. Furthermore, we demonstrate that bone tissue that forms in response to the physical topographical features of nacre has a higher crystallinity than bone formed in response to chemical cues with a full width half-maximum for PO43- Raman shift of 7.6 ± 0.7 for mineral produced in response to nacre replica compared to a much broader 34.6 ± 10.1 in response to standard osteoinductive medium. These differences in mineral product are underpinned by differences in cellular metabolism. This observation can be exploited in the design of bone therapies; a matter that is most pressing in light of a rapidly aging human population.
Highlights
Aragonite and calcite are the two calcium carbonate polymorphs that constitute the shell of molluscan bivalves conferring strength and resilience due to the nano- and microstructural assembly of the overall architecture.[1]
By isolating the topographical features of nacre from its inherent chemistry, we show that the osteoinductive properties of nacre arise from the patterning of the surface presented to mesenchymal stem cells (MSCs)
Mean surface roughness measurements (n = 6) of nacre and the nacre replica surface averaged at 221.8 ± 19 nm and 235.1 ± 47.9 nm, respectively, showing no significant difference between the original and replica surfaces (Figure 1B)
Summary
Aragonite and calcite are the two calcium carbonate polymorphs that constitute the shell of molluscan bivalves conferring strength and resilience due to the nano- and microstructural assembly of the overall architecture.[1]. The discovery of fully integrated shell dental implants in Mayan skulls[9] initiated a number of studies showing that nacre, or mother of pearl, the aragonite calcium carbonate polymorph derived from the pearl oyster Pinctada maxima has good osteointegrative properties in vivo.[10−13] Further exploration of this phenomenon in human jaw reconstructions and sheep femur implants[10,11,14] confirms the osteointegrative properties of invertebrate shells. OPN expression levels increased over time on the nacre replica surfaces indicating osteogenic development. Cells cultured in differentiating media and on nacre replica topography showing increased expression of osteopontin (green) compared to undifferentiated cells on the planar substrate. Differentiation in mesenchymal stem cells (MSCs) in vitro.[15−17] This observation has led to a number of studies in which nacre and its chemistry have been incorporated into the design of existing biomaterials to induce bone formation.[15,18−20]
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